Interaction of the Salmonella-containing Vacuole with the Endocytic Recycling System

Upon entry of the pathogen Salmonella enterica serovar Typhimurium into host cells, the majority of bacteria reside in a membrane-bound compartment called the Salmonella-containing vacuole (SCV). Previous studies have established that the SCV transiently interacts with early endosomes but only acquires a subset of late endosomal/lysosomal proteins. However, the complete set of interactions between the SCV and the endocytic machinery has yet to be characterized. In this study, we have shown that four characterized regulators of endocytic recycling were present on the SCV after invasion. Interaction kinetics were different for each of the regulators; ARF6 and Rab4 associated immediately, but their presence was diminished 60 min post-infection, whereas syntaxin13 and Rab11 association peaked at 60 min. Using a dominant negative approach, we determined that Rab11 regulates the recycling of CD44 from the vacuole but had no effect on major histocompatibility complex (MHC) class I recycling. In contrast, syntaxin13 regulated the recycling of MHC class I but not of CD44. We also determined that maturation of the SCV, measured by the acquisition of lysosomal associated membrane protein-1, slowed when recycling was impaired. These findings suggest that protein movement through the endocytic recycling system is regulated through at least two concurrent pathways and that efficient interaction with these pathways is necessary for maturation of the Salmonella-containing vacuole. We also demonstrate the utility of using Salmonella invasion as a model of endosomal recycling events. Upon entry of the pathogen Salmonella enterica serovar Typhimurium into host cells, the majority of bacteria reside in a membrane-bound compartment called the Salmonella-containing vacuole (SCV). Previous studies have established that the SCV transiently interacts with early endosomes but only acquires a subset of late endosomal/lysosomal proteins. However, the complete set of interactions between the SCV and the endocytic machinery has yet to be characterized. In this study, we have shown that four characterized regulators of endocytic recycling were present on the SCV after invasion. Interaction kinetics were different for each of the regulators; ARF6 and Rab4 associated immediately, but their presence was diminished 60 min post-infection, whereas syntaxin13 and Rab11 association peaked at 60 min. Using a dominant negative approach, we determined that Rab11 regulates the recycling of CD44 from the vacuole but had no effect on major histocompatibility complex (MHC) class I recycling. In contrast, syntaxin13 regulated the recycling of MHC class I but not of CD44. We also determined that maturation of the SCV, measured by the acquisition of lysosomal associated membrane protein-1, slowed when recycling was impaired. These findings suggest that protein movement through the endocytic recycling system is regulated through at least two concurrent pathways and that efficient interaction with these pathways is necessary for maturation of the Salmonella-containing vacuole. We also demonstrate the utility of using Salmonella invasion as a model of endosomal recycling events. Salmonella enterica serovar Typhimurium (Salmonella Typhimurium) is a facultative intracellular pathogen responsible for disease across species, ranging from gastroenteritis to enteric fever (1Tsolis R.M. Kingsley R.A. Townsend S.M. Ficht T.A. Adams L.G. Baumler A.J. Adv. Exp. Med. Biol. 1999; 473: 261-274Crossref PubMed Google Scholar). Invasion into the intestinal epithelia of the host is modeled in vitro using epithelial cell cultures, which have provided a wealth of information regarding the pathogenesis of Salmonella Typhimurium (reviewed by Hurley and McCormick) (2Hurley B.P. McCormick B.A. Trends Microbiol. 2003; 11: 562-569Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar). Uptake into epithelial cells is directed through the Salmonella pathogenicity island (SPI) 1The abbreviations used are: SPI, Salmonella pathogenicity island; ARF, ADP ribosylation factor; EGFP, enhanced green fluorescent protein; HA, hemagglutinin; LAMP, lysosomal associated membrane protein; MHC, major histocompatability complex; NSF, N-ethylmaleimide sensitive factor; PBS, phosphate-buffered saline; p.i., post-infection; SCV, Salmonella-containing vacuole; SNARE, soluble N-ethylmaleimide sensitive factor attachment protein receptor. 1 type III secretion system, a needle-like device protruding from the bacterial cell wall that delivers bacterial virulence proteins into host cells (3Hueck C.J. Microbiol. Mol. Biol. Rev. 1998; 62: 379-433Crossref PubMed Google Scholar). The virulence proteins, called effectors, are translocated from the bacteria into the host cytosol where they direct actin rearrangements leading to membrane ruffling, which results in uptake of the bacteria (4Galan J.E. Zhou D. Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 8754-8761Crossref PubMed Scopus (217) Google Scholar). Once inside, the bacteria reside in a membrane-bound compartment called the Salmonella-containing vacuole (SCV) and establish a replicative niche. Recently, an active SPI-1 system has been shown to be necessary for the intracellular survival and replication of Salmonella Typhimurium in epithelial cells (5Steele-Mortimer O. Brumell J.H. Knodler L.A. Meresse S. Lopez A. Finlay B.B. Cell. Microbiol. 2002; 4: 43-54Crossref PubMed Scopus (172) Google Scholar). Early in the infection of epithelial cells (up to ∼15 min), trafficking of the SCV resembles that of model phagosomes (reviewed by Brumell and Grinstein) (6Brumell J.H. Grinstein S. Curr. Opin. Microbiol. 2004; 7: 78-84Crossref PubMed Scopus (99) Google Scholar). Markers such as the early endosome antigen-1 (7Steele-Mortimer O. Méresse S. Gorvel J-P. Toh B.-H. Finlay B.B. Cell. Microbiol. 1999; 1: 33-51Crossref PubMed Scopus (262) Google Scholar) and the GTPase Rab5 (8Roberts R.L. Barbieri M.A. Ullrich J. Stahl P.D. J. Leukocyte Biol. 2000; 68: 627-632PubMed Google Scholar) are transiently present on the SCV, indicative of interactions with early endosomes. These are rapidly removed, followed by the acquisition of several late endosome/lysosome markers, including Rab7 (9Meresse S. Steele-Mortimer O. Finlay B.B. Gorvel J.P. EMBO J. 1999; 18: 4394-4403Crossref PubMed Scopus (202) Google Scholar) and lysosomal membrane glycoproteins (10Garcia-del Portillo F. Finlay B.B. J. Cell Biol. 1995; 129: 81-97Crossref PubMed Scopus (209) Google Scholar). Interestingly, acquisition of lysosomal associated membrane protein-1 (LAMP-1) is dependent on Rab7 activity (9Meresse S. Steele-Mortimer O. Finlay B.B. Gorvel J.P. EMBO J. 1999; 18: 4394-4403Crossref PubMed Scopus (202) Google Scholar); yet, despite the presence of active Rab7 on the early SCV (11Harrison R.E. Brumell J.H. Khandani A. Bucci C. Scott C.C. Jiang X. Finlay B.B. Grinstein S. Mol. Biol. Cell. 2004; 15: 3146-3154Crossref PubMed Scopus (134) Google Scholar), the bacteria avoid or delay fusion with late endosomes/lysosomes that carry LAMP-1. This is shown by the lack of mannose-6-phosphate receptor, cathepsin D, and lysobisphosphatidic acid on the SCV during the first 3 h post-infection (p.i.) (10Garcia-del Portillo F. Finlay B.B. J. Cell Biol. 1995; 129: 81-97Crossref PubMed Scopus (209) Google Scholar, 12Brumell J.H. Tang P. Mills S.D. Finlay B.B. Traffic. 2001; 2: 643-653Crossref PubMed Scopus (101) Google Scholar). Understanding the pathways behind these events may lead to an elucidation of the mechanisms Salmonella Typhimurium uses to direct its intracellular fate in host cells. To do this, it is necessary to characterize the interactions of the SCV with the host endocytic system from invasion onward. The ruffling that occurs during Salmonella invasion induces the internalization of plasma membrane to form the SCV as well as other endosomes. These endosomes can be empty or they may contain nearby Salmonella or inert “bystander” particles (13Francis C.L. Ryan T.A. Jones B.D. Smith S.J. Falkow S. Nature. 1993; 364: 639-642Crossref PubMed Scopus (357) Google Scholar, 14Garcia-del Portillo F. Finlay B.B. Infect. Immun. 1994; 62: 4641-4645Crossref PubMed Google Scholar, 15Terebiznik M.R. Vieira O.V. Marcus S.L. Slade A. Yip C.M. Trimble W.S. Meyer T. Finlay B.B. Grinstein S. Nat. Cell Biol. 2002; 4: 766-773Crossref PubMed Scopus (231) Google Scholar). Included on the SCV and surrounding endosomes are plasma membrane proteins that have been shown to aggregate at the site of invasion (16Garcia-del Portillo F. Pucciarelli M.G. Jefferies W.A. Finlay B.B. J. Cell Sci. 1994; 107: 2005-2020Crossref PubMed Google Scholar). Two such proteins are major histocompatibility complex (MHC) class I, involved in the presentation of peptides to T cells (17Townsend A.R. Gotch F.M. Davey J. Cell. 1985; Full Text PDF PubMed Scopus Google Scholar), and the for acid involved in S.M. Full Text PDF PubMed Scopus Google Scholar). The presence of these proteins on the of the SCV (16Garcia-del Portillo F. Pucciarelli M.G. Jefferies W.A. Finlay B.B. J. Cell Sci. 1994; 107: 2005-2020Crossref PubMed Google Scholar), that active recycling is recycling is necessary for maturation Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar, A.J. Traffic. 2004; PubMed Scopus Google Scholar), but its in SCV maturation recycling is a complex and trafficking events (reviewed by and Nat. Rev. Mol. Cell Biol. 2004; PubMed Scopus Google Scholar). of this protein including proteins, involved in These proteins four and by proteins to a membrane (reviewed by and Nat. Rev. Mol. Cell Biol. 2001; 2: PubMed Scopus Google Scholar). Rab4 to early endosomes and regulates early events from S. J. J. Cell Biol. 2000; PubMed Scopus Google Scholar, J. Cell Biol. 1999; PubMed Scopus Google Scholar). Rab11 to the S. J. J. Cell Biol. 2000; PubMed Scopus Google Scholar, Ullrich O. J. Cell Sci. 1999; PubMed Google Scholar) and is involved in recycling to the plasma membrane or the J. Cell Biol. 1999; PubMed Scopus Google Scholar, D. A. Mol. Biol. Cell. 1998; PubMed Scopus Google Scholar, J. C. Proc. Natl. Acad. Sci. U. S. A. 1998; PubMed Scopus Google Scholar, O. S. S. J. Cell Biol. PubMed Scopus Google Scholar). The ribosylation protein of also as regulators of membrane (reviewed by and P. Curr. Opin. Cell Biol. 1999; 11: PubMed Scopus Google Scholar). ARF6 in the plasma system C. Stahl P.D. 1995; PubMed Scopus Google Scholar, D. J. Cell Biol. 1995; PubMed Scopus Google Scholar) and is involved in recycling and to of the plasma membrane T. J. Cell Biol. 2001; PubMed Scopus Google Scholar, J. Cell Biol. PubMed Scopus Google Scholar, C. C. Stahl P.D. J. Cell Biol. 1998; PubMed Scopus Google Scholar, J. J. A. Traffic. 2004; PubMed Scopus Google Scholar, T. D. C. J. P. J. Cell Biol. 2003; PubMed Scopus Google Scholar). are soluble factor attachment protein involved in and fusion (reviewed by and Nat. Rev. Mol. Cell Biol. 2001; 2: PubMed Scopus Google Scholar). to the and is involved in the fusion events for recycling Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar, J. J. Cell Biol. 1998; PubMed Scopus Google Scholar). Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar) have shown that active syntaxin13 is necessary for maturation of the of endocytic recycling have shown that is to through different pathways S. J. J. Cell Biol. 2000; PubMed Scopus Google Scholar, J. Cell Biol. 1999; PubMed Scopus Google Scholar, A. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, M.A. J. A. S.M. Mol. Biol. Cell. 2001; PubMed Scopus Google Scholar, S. J. Cell Biol. 1993; PubMed Scopus Google Scholar). However, it is not which regulators are for which or which we characterized the interaction of recycling proteins with the we that recycling from the SCV through at least two concurrent pathways that are by syntaxin13 and we that active recycling is for efficient maturation of the These the utility of using Salmonella Typhimurium as a model for the of membrane recycling events in cells. Cell and epithelial cell cells were from the were in with at in were used between type Salmonella Typhimurium B.A. Nature. PubMed Scopus Google Scholar) was used in this and ARF6 was as J.E. Mol. Biol. Cell. 1998; PubMed Scopus Google Scholar, S. Tang S. F. J. Cell Biol. 1999; PubMed Scopus Google Scholar). and have been M.A. Infect. Immun. 2003; PubMed Scopus Google Scholar). was using using as a with the and the and were from Trimble of and the of Cell for Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar). The was used for of cells with to the CD44 and were from were from to Salmonella Typhimurium were from were from were from by T. were from the the of the of and by The of of The used were and from of Cell epithelial cells were at in h cells were h bacterial were used for cells and using a for bacterial invasion (7Steele-Mortimer O. Méresse S. Gorvel J-P. Toh B.-H. Finlay B.B. Cell. Microbiol. 1999; 1: 33-51Crossref PubMed Scopus (262) Google Scholar). In bacteria were for h at with and in for 3 were by at for in and to cells at a of infection of at for min. bacteria were by with and the of min of bacterial the was to were in in PBS, for min at cells were with and by with in for min. and were on in for min to 1 followed by with were using fluorescent were using a were into in and in was used to the association of different proteins with the The of SCV with each host cell protein was as the between bacteria the host cell protein and the of was determined with a surrounding the bacteria This was determined for at least The S.D. for at least is cell cells were with and as with Salmonella Typhimurium the protein from the provided by J. F. J. Microbiol. 2004; PubMed Scopus Google Scholar). were on a with a were through the of the were with cells at in to with bacterial a was used to the of bacteria The of intracellular bacteria was for at least cells. The S.D. for is Salmonella Invasion of Cell in invasion of epithelial cells is in that it is a bacterial (reviewed by Brumell J.H. Steele-Mortimer O. Finlay B.B. Curr. Biol. 1999; Full Text Full Text PDF PubMed Scopus Google Scholar). Invasion has been as to invasion of bacteria a ruffling of the cell that the of other bacteria into as well as the of endosomes (13Francis C.L. Ryan T.A. Jones B.D. Smith S.J. Falkow S. Nature. 1993; 364: 639-642Crossref PubMed Scopus (357) Google Scholar, 14Garcia-del Portillo F. Finlay B.B. Infect. Immun. 1994; 62: 4641-4645Crossref PubMed Google Scholar, 15Terebiznik M.R. Vieira O.V. Marcus S.L. Slade A. Yip C.M. Trimble W.S. Meyer T. Finlay B.B. Grinstein S. Nat. Cell Biol. 2002; 4: 766-773Crossref PubMed Scopus (231) Google Scholar). Previous has shown that the MHC class I and CD44 with the SCV the invasion of epithelial cells (16Garcia-del Portillo F. Pucciarelli M.G. Jefferies W.A. Finlay B.B. J. Cell Sci. 1994; 107: 2005-2020Crossref PubMed Google Scholar). In a of each is during the invasion and on endosomes the site of bacterial entry (16Garcia-del Portillo F. Pucciarelli M.G. Jefferies W.A. Finlay B.B. J. Cell Sci. 1994; 107: 2005-2020Crossref PubMed Google Scholar). This is in cells were with type Salmonella Typhimurium or min p.i., and for bacteria and for MHC class I or CD44. of MHC class I proteins was at the site of bacterial entry min after infection that was not present in cells In MHC class I with the SCV for CD44 a with of in the of bacterial entry and a direct with the SCV after min In on endosomes was or no present after min and and was with the This of cell proteins from the SCV and endosomes active recycling events on these of to the the by which CD44 and MHC class I are from the SCV, we recycling regulators were present on this associated transiently with the SCV with association at min and it was no present after 60 min ARF6 with the SCV min p.i., but was after 60 min in cells with and bacterial ARF6 was present on membrane not recycling regulators syntaxin13 and To the cells transiently with were and to was in the and in the with Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar, J. J. Cell Biol. 1998; PubMed Scopus Google Scholar). However, cells min that intracellular bacteria with with the SCV and min the had and the majority of no with and Rab11 and in cells with a with S. J. J. Cell Biol. 2000; PubMed Scopus Google Scholar, Ullrich O. J. Cell Sci. 1999; PubMed Google Scholar). at min an of Rab11 the bacteria as well as with the SCV min the was no present and with the SCV had diminished The kinetics of Rab11 with the SCV association 60 min and to by min interactions of the SCV with recycling each kinetics of association with the syntaxin13 and Rab11 a of protein from the to the the SCV and 3 from of cells in the of this The majority of was in the min min p.i., to to the site of bacterial min the majority of was the and this to 60 min. findings demonstrate that a of the endosomal system occurs during characterized by of recycling to the SCV and surrounding endosomes at the site of bacterial and Rab11 of Cell from the the presence of syntaxin13 and Rab11 on the SCV with the of CD44 and MHC class I we set to these recycling a in the of cell proteins from the To the of syntaxin13 in a dominant negative a of which is to form a complex with the Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar) was with with of cells when a cells were and for bacteria and for MHC class I or CD44. of MHC class I was present in cells and in cells at min and However, cells the of MHC class I proteins in cells to min in cells. a dominant negative form of syntaxin13 to an of as shown by the of MHC class I proteins. To this we of the well vacuole by Salmonella The presence or of MHC class I on the SCV was a of recycling from a vacuole. of association MHC class I with cells after but cells the had with MHC class I at 60 and min was the in cells and in at min These findings are with the effect of this on the of MHC class I proteins the in the recycling be to delay the of cell from the of endosomal membrane the SCV, and of these in syntaxin13 a in the recycling of MHC class of CD44 that in the of the SCV was present in after min and had by min and In with the SCV no between and cells This that syntaxin13 or no in the recycling of CD44. we the of Rab11 in the recycling of cell proteins from the We cells with to with dominant negative O. S. S. J. Cell Biol. PubMed Scopus Google Scholar). MHC class I in cells was with cells The of MHC class I proteins at the site of bacterial invasion was present after min and had by min. association of MHC class I with the SCV was to be by the of However, when CD44 in cells, we the SCV present at and min after infection This was in to cells, where of CD44 was by min of CD44 with the SCV was min in Rab11 dominant cells in cells. The was the Rab11 a in but not MHC class I, recycling. In these findings that recycling pathways the recycling of cell proteins from the and Rab11 for of the recycling pathways a in maturation of the SCV, we used a dominant negative and the of on the has been used as a of SCV maturation (9Meresse S. Steele-Mortimer O. Finlay B.B. Gorvel J.P. EMBO J. 1999; 18: 4394-4403Crossref PubMed Scopus (202) Google Scholar, Portillo F. Finlay B.B. J. Cell Biol. 1995; 129: 81-97Crossref PubMed Scopus (209) Google Scholar, Meresse S. C. Gorvel J.P. Cell Microbiol. 2001; PubMed Scopus Google Scholar). cells were with Salmonella and were for the presence or of LAMP-1. was not present on the SCV min after invasion with (9Meresse S. Steele-Mortimer O. Finlay B.B. Gorvel J.P. EMBO J. 1999; 18: 4394-4403Crossref PubMed Scopus (202) Google Scholar) in cells with or of the dominant negative not However, was rapidly on in cells during a of or the of with cells of dominant negative had an the of to the of in cells at 60 min and To that or the of dominant negative not the of bacteria in the we a infection and for a of bacteria A.J. Jiang X. C.L. Brumell J.H. Curr. Biol. 2004; Full Text Full Text PDF PubMed Scopus Google Scholar). We not an of bacteria in the cytosol not In study, the in is to the recycling activity and not to of the findings demonstrate that recycling activity is for efficient maturation of the We to recycling is for bacterial replication of Salmonella Typhimurium is dependent on a type III secretion system in Falkow S. Mol. Microbiol. 1998; PubMed Scopus Google Scholar, J.E. T. A. C. Mol. Microbiol. 1998; PubMed Scopus Google Scholar, F. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). associated with is the of M.A. Portillo F. Finlay B.B. Mol. Microbiol. PubMed Scopus Google Scholar), which we have shown are associated with rapidly bacteria C.L. Jiang X. Brumell J.H. Infect. Immun. PubMed Scopus Google Scholar). to recycling regulators the replication of Salmonella we to these proteins were present on and that they were not not we the activity of syntaxin13 and Rab11 in cells using the dominant negative and the of Salmonella Typhimurium bacteria cell an We no in the of Salmonella Typhimurium bacteria cell the not of Rab11 and syntaxin13 not the replication of Salmonella Typhimurium in cells. is well established that Salmonella Typhimurium can maturation of the SCV to a replicative in cells of its However, the complete set of interactions that between the SCV and the host cell endosomal system is we have the association of endocytic recycling regulators with the SCV in cells, recycling pathways and the of recycling in SCV The association of recycling regulators with the SCV is of their association with Rab4 has been shown to with early endosomes and recycling to the plasma membrane S. J. J. Cell Biol. 2000; PubMed Scopus Google Scholar, J. Cell Biol. 1999; PubMed Scopus Google Scholar). an interaction of Rab4 with the SCV early in infection min), followed by a from the These with maturation of the SCV as characterized by of early endosome 1 (7Steele-Mortimer O. Méresse S. Gorvel J-P. Toh B.-H. Finlay B.B. Cell. Microbiol. 1999; 1: 33-51Crossref PubMed Scopus (262) Google Scholar). also present on the SCV early in is involved in recycling to of membrane J. J. A. Traffic. 2004; PubMed Scopus Google Scholar, T. D. C. J. P. J. Cell Biol. 2003; PubMed Scopus Google Scholar). The interaction of ARF6 with the SCV may be a to the membrane rearrangements of internalization of Salmonella the presence of ARF6 on membrane with a the of ARF6 in a by Salmonella J.E. McCormick B.A. J. Biol. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). has a for ARF6 in the recycling of MHC class I through a from the recycling complex J. Cell Biol. PubMed Scopus Google Scholar). the of ARF6 on the membrane of the SCV during the of MHC class I recycling was we that it not a in the recycling of MHC class I from the SCV in cells. this it is not Rab4 and ARF6 in of recycling from the and Rab11 have been shown to recycling through the recycling complex Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar, J. Cell Biol. 1999; PubMed Scopus Google Scholar, D. A. Mol. Biol. Cell. 1998; PubMed Scopus Google Scholar, J. C. Proc. Natl. Acad. Sci. U. S. A. 1998; PubMed Scopus Google Scholar, O. S. S. J. Cell Biol. PubMed Scopus Google Scholar, J. J. Cell Biol. 1998; PubMed Scopus Google Scholar). In study, proteins interaction with the SCV min p.i., which with a Rab11 interaction with endosomes min after internalization O. S. S. J. Cell Biol. PubMed Scopus Google Scholar). However, this a syntaxin13 interaction with phagosomes min after internalization Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar). This in kinetics may be to in cell type of entry invasion We have shown that MHC class I and CD44 were in a and pathways for recycling of from endosomes have been recycling from the endosome by Rab4 S. J. J. Cell Biol. 2000; PubMed Scopus Google Scholar, J. Cell Biol. 1999; PubMed Scopus Google Scholar), a recycling through the recycling compartment S. J. Cell Biol. 1993; PubMed Scopus Google Scholar), and a through the recycling compartment A. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar, M.A. J. A. S.M. Mol. Biol. Cell. 2001; PubMed Scopus Google Scholar). through the has a of min A. J. Biol. 1998; Full Text Full Text PDF PubMed Scopus Google Scholar), to the of MHC class I and CD44 recycling from the SCV suggest that the two pathways of recycling and at least in by syntaxin13 and The association of the SCV with MHC class I may suggest a for syntaxin13 in and associated with MHC class I of peptides in an compartment has been T. Zhou X. C. J. 1995; Google Scholar, 1995; Google Scholar, J. J. PubMed Scopus Google Scholar, J. J. 1995; PubMed Scopus Google Scholar, J. Google Scholar, J. PubMed Scopus Google Scholar). can be endosomes A. T. C.J. S. J. Google Scholar, J.H. Jiang J. Google Scholar), and MHC class I can to the cell J. A. D. J. Proc. Natl. Acad. Sci. U. S. A. 1999; PubMed Scopus Google Scholar). on the internalization of MHC class I infection with Salmonella it is that bacterial are as MHC class I is with the SCV and are to the plasma membrane for that syntaxin13 a in MHC class I recycling to the cell The of has been used to the maturation of the SCV to a late compartment (9Meresse S. Steele-Mortimer O. Finlay B.B. Gorvel J.P. EMBO J. 1999; 18: 4394-4403Crossref PubMed Scopus (202) Google Scholar, Portillo F. Finlay B.B. J. Cell Biol. 1995; 129: 81-97Crossref PubMed Scopus (209) Google Scholar, Meresse S. C. Gorvel J.P. Cell Microbiol. 2001; PubMed Scopus Google Scholar). findings dominant negative recycling that with recycling maturation of the SCV, as characterized by a delay in This is with results the of dominant negative syntaxin13 on maturation of phagosomes in Grinstein S. Trimble W.S. J. 2002; PubMed Scopus Google Scholar). is an effect on it is not of complete the study, the of dominant negative only a in recycling or This the presence of recycling pathways or we the replication of Salmonella Typhimurium in cells, we no in replication not that pathways are to complete the necessary recycling in for replication to In that the SCV interacts with recycling we that Rab11 and syntaxin13 concurrent We have also shown that recycling and maturation are with the of cell we that early trafficking of the SCV can be used as a model of endocytic recycling. are to be regarding the trafficking of the SCV, and a to a complete set of interactions with the machinery is to these We are to and for for with and and for and of this with

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